Memory and naive-like regulatory CD4 + T cells expand during HIV-2 infection in direct association with CD4 + T-cell depletion irrespectively of viremia

AIDS

Volumn 25, Issue 16, 2011, Pages 1961-1970

  Foxall, Russell B ^a   Albuquerque, Adriana S ^a   Soares, Rui S ^a   Baptista, António P ^a,d   Cavaleiro, Rita ^a   Tendeiro, Rita ^a   Gomes, Perpétua ^b   Victorino, Rui M M ^a,c   Sousa, Ana E ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b HOSPITAL EGAS MONIZ   (Portugal)

^c HOSPITAL DE SANTA MARIA   (Portugal)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

HIV 2; HIV AIDS; immune activation; regulatory T cells

Indexed keywords

CD4 ANTIGEN; KI 67 ANTIGEN; TRANSCRIPTION FACTOR FOXP3;

ADULT; AGED; AIDS PATIENT; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTOPENIA; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SERODIAGNOSIS; T CELL DEPLETION; VIREMIA;

ADULT; AGED; CROSS-SECTIONAL STUDIES; DISEASE PROGRESSION; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HIV-2; HUMANS; IMMUNOPHENOTYPING; MALE; MIDDLE AGED; PHENOTYPE; T-LYMPHOCYTES, REGULATORY; VIREMIA;

EID: 80054967903     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32834b3554     Document Type: Article

References (48)

1. Shen S, Ding Y, Tadokoro CE, Olivares-Villagomez D, Camps-Ramirez M, Curotto de Lafaille MA, Lafaille JJ. Control of homeostatic proliferation by regulatory T cells. J Clin Invest 2005; 115:3517-3526. (Pubitemid 43121839)
2. Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 2007; 7:875-888. (Pubitemid 350006238)
3. Boettler T, Spangenberg HC, Neumann-Haefelin C, Panther E, Urbani S, Ferrari C, et al. T cells with a CD4RCD25R regulatory phenotype suppress in vitro proliferation of virus-specific CD8R T cells during chronic hepatitis C virus infection. J Virol 2005; 79:7860-7867. (Pubitemid 40756821)
4. Bolacchi F, Sinistro A, Ciaprini C, Demin F, Capozzi M, Carducci FC, et al. Increased hepatitis C virus (HCV)-specific CD4RCD25R regulatory T lymphocytes and reduced HCVspecific CD4R T cell response in HCV-infected patients with normal versus abnormal alanine aminotransferase levels. Clin Exp Immunol 2006; 144:188-196.
5. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4R T-cell changes independent of viral load. Blood 2004; 104:942-947. (Pubitemid 39038012)
6. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, Lange JM, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 2003; 17:1881-1888. (Pubitemid 37070273)
7. Rodriguez B, Sethi AK, Cheruvu VK, Mackay W, Bosch RJ, Kitahata M, et al. Predictive value of plasma HIV RNA level on rate of CD4 T-cell decline in untreated HIV infection. JAMA 2006; 296:1498-1506. (Pubitemid 44465514)
8. Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF. Human CD4R CD25R regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J Virol 2004; 78:2454-2459. (Pubitemid 38228938)
9. Kinter AL, Hennessey M, Bell A, Kern S, Lin Y, Daucher M, et al. CD25(R)CD4(R) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(R) and CD8(R) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med 2004; 200:331-343. (Pubitemid 39031252)
10. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, Levy Y. Human immunodeficiency virus-driven expansion of CD4RCD25R regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 2004; 104:3249-3256. (Pubitemid 39507143)
11. Kinter AL, Horak R, Sion M, Riggin L, McNally J, Lin Y, et al. CD25R regulatory T cells isolated from HIV-infected individuals suppress the cytolytic and nonlytic antiviral activity of HIV-specific CD8R T cells in vitro. AIDS Res Hum Retroviruses 2007; 23:438-450. (Pubitemid 46608564)
12. Kinter A, McNally J, Riggin L, Jackson R, Roby G, Fauci AS. Suppression of HIV-specific T cell activity by lymph node CD25R regulatory T cells from HIV-infected individuals. Proc Natl Acad Sci USA 2007; 104:3390-3395. (Pubitemid 46364169)
13. Epple HJ, Loddenkemper C, Kunkel D, Troger H, Maul J, Moos V, et al. Mucosal but not peripheral FOXP3R regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood 2006; 108:3072-3078.
14. Nilsson J, Boasso A, Velilla PA, Zhang R, Vaccari M, Franchini G, et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 2006; 108:3808-3817. (Pubitemid 44864563)
15. Andersson J, Boasso A, Nilsson J, Zhang R, Shire NJ, Lindback S, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol 2005; 174:3143-3147. (Pubitemid 40354012)
16. Baker CA, Clark R, Ventura F, Jones NG, Guzman D, Bangsberg DR, Cao H. Peripheral CD4 loss of regulatory T cells is associated with persistent viraemia in chronic HIV infection. Clin Exp Immunol 2007; 147:533-539. (Pubitemid 46208056)
17. Eggena MP, Barugahare B, Jones N, Okello M, Mutalya S, Kityo C, et al. Depletion of regulatory T cells in HIV infection is associated with immune activation. J Immunol 2005; 174: 4407-4414. (Pubitemid 40396024)
18. Schulze Zur Wiesch J, Thomssen A, Hartjen P, Toth I, Lehmann C, Meyer-Olson D, et al. Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3R T regulatory cells correlates with progressive disease. J Virol 2011; 85:1287-1297.
19. Popper SJ, Sarr AD, Gueye-Ndiaye A, Mboup S, Essex ME, Kanki PJ. Low plasma human immunodeficiency virus type 2 viral load is independent of proviral load: low virus production in vivo. J Virol 2000; 74:1554-1557. (Pubitemid 30044108)
20. Drylewicz J, Matheron S, Lazaro E, Damond F, Bonnet F, Simon F, et al. Comparison of viro-immunological marker changes between HIV-1 and HIV-2-infected patients in France. AIDS 2008; 22:457-468. (Pubitemid 351317287)
21. Marlink R, Kanki P, Thior I, Travers K, Eisen G, Siby T, et al. Reduced rate of disease development after HIV-2 infection as compared to HIV-1. Science 1994; 265:1587-1590. (Pubitemid 24308975)
22. Poulsen AG, Aaby P, Larsen O, Jensen H, Naucler A, Lisse IM, et al. 9-year HIV-2-associated mortality in an urban community in Bissau, west Africa. Lancet 1997; 349:911-914. (Pubitemid 27139820)
23. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 2002; 169:3400-3406. (Pubitemid 35013190)
24. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE. CD4RT-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med 2002; 8:319-323. (Pubitemid 34407019)
25. Aiuti F, Mezzaroma I. Failure to reconstitute CD4R T-cells despite suppression of HIV replication under HAART. AIDS Rev 2006; 8:88-97. (Pubitemid 44043557)
26. Marchetti G, Gori A, Casabianca A, Magnani M, Franzetti F, Clerici M, et al. Comparative analysis of T-cell turnover and homeostatic parameters in HIV-infected patients with discordant immune-virological responses to HAART. AIDS 2006; 20:1727-1736. (Pubitemid 44299364)
27. Soares R, Foxall R, Albuquerque A, Cortesao C, Garcia M, Victorino RM, Sousa AE. Increased frequency of circulating CCR5RCD4RT cells in human immunodeficiency virus type 2 infection. J Virol 2006; 80:12425-12429. (Pubitemid 44904396)
28. Albuquerque AS, Foxall RB, Cortesao CS, Soares RS, Doroana M, Ribeiro A, et al. Low CD4 T-cell counts despite low levels of circulating HIV: insights from the comparison of HIV-1 infected patients with a discordant response to antiretroviral therapy to patients with untreated advanced HIV-2 disease. Clin Immunol 2007; 125:67-75. (Pubitemid 47376925)
29. Foxall RB, Soares RS, Albuquerque AS, Cortesao CS, Victorino RM, Sousa AE. Increased frequency of CD25dimCD4R T-cells in HIV-2 infection, a naturally occurring attenuated form of HIV-1. Clin Immunol 2008; 127:158-167.
30. Soriano V, Gomes P, Heneine W, Holguin A, Doruana M, Antunes R, et al. Human immunodeficiency virus type 2 (HIV-2) in Portugal: clinical spectrum, circulating subtypes, virus isolation, and plasma viral load. J Med Virol 2000; 61:111-116. (Pubitemid 30191235)
31. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4RCD25high regulatory cells in human peripheral blood. J Immunol 2001; 167:1245-1253. (Pubitemid 32703119)
32. Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, Niwa A, et al. Functional delineation and differentiation dynamics of human CD4R T cells expressing the FoxP3 transcription factor. Immunity 2009; 30:899-911.
33. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061. (Pubitemid 36222930)
34. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4RFOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007; 110:2983-2990. (Pubitemid 350006952)
35. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4R T cells. Eur J Immunol 2007; 37:129-138. (Pubitemid 46128793)
36. Del Pozo-Balado Mdel M, Leal M, Mendez-Lagares G, Pacheco YM. CD4(R)CD25(R/hi)CD127(lo) phenotype does not accurately identify regulatory T cells in all populations of HIV-infected persons. J Infect Dis 2010; 201:331-335.
37. Albuquerque AS, Cortesao CS, Foxall RB, Soares RS, Victorino RM, Sousa AE. Rate of increase in circulating IL-7 and loss of IL-7Ralpha expression differ in HIV-1 and HIV-2 infections: two lymphopenic diseases with similar hyperimmune activation but distinct outcomes. J Immunol 2007; 178:3252-3259. (Pubitemid 46333208)
38. Grabar S, Selinger-Leneman H, Abgrall S, Pialoux G, Weiss L, Costagliola D. Prevalence and comparative characteristics of long-term nonprogressors and HIV controller patients in the French Hospital Database on HIV. AIDS 2009; 23:1163-1169.
39. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, et al. Shorter survival in advanced human immunodeficiency virus type1 infection ismore closely associated withT lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 1999; 179:859-870. (Pubitemid 29159331)
40. Booth NJ, McQuaid AJ, Sobande T, Kissane S, Agius E, Jackson SE, et al. Different proliferative potential and migratory characteristics of human CD4R regulatory T cells that express either CD45RA or CD45RO. J Immunol 2010; 184:4317-4326.
41. Benveniste O, Flahault A, Rollot F, Elbim C, Estaquier J, Pedron B, et al. Mechanisms involved in the low-level regeneration of CD4R cells in HIV-1-infected patients receiving highly active antiretroviral therapy who have prolonged undetectable plasma viral loads. J Infect Dis 2005; 191:1670-1679. (Pubitemid 40656755)
42. Teixeira L, Valdez H, McCune JM, Koup RA, Badley AD, Hellerstein MK, et al. Poor CD4 T cell restoration after suppression of HIV-1 replication may reflect lower thymic function. AIDS 2001; 15:1749-1756. (Pubitemid 32939234)
43. Roederer M, Dubs JG, Anderson MT, Raju PA, Herzenberg LA. CD8 naive T cell counts decrease progressively in HIV-infected adults. J Clin Invest 1995; 95:2061-2066.
44. Vukmanovic-Stejic M, Zhang Y, Cook JE, Fletcher JM, McQuaid A, Masters JE, et al. Human CD4R CD25hi Foxp3R regulatory T cells are derived by rapid turnover of memory populations in vivo. J Clin Invest 2006; 116:2423-2433. (Pubitemid 44330141)
45. Mabarrack NH, Turner NL, Mayrhofer G. Recent thymic origin, differentiation, and turnover of regulatory T cells. J Leukoc Biol 2008; 84:1287-1297.
46. Bandera A, Ferrario G, Saresella M, Marventano I, Soria A, Zanini F, et al. CD4R T cell depletion, immune activation and increased production of regulatory T cells in the thymus of HIV-infected individuals. PLoS One 2010; 5:e10788.
47. Marziali M, De Santis W, Carello R, Leti W, Esposito A, Isgro A, et al. T-cell homeostasis alteration in HIV-1 infected subjects with low CD4 T-cell count despite undetectable virus load during HAART. AIDS 2006; 20:2033-2041. (Pubitemid 44611056)
48. Isgro A, Leti W, De Santis W, Marziali M, Esposito A, Fimiani C, et al. Altered clonogenic capability and stromal cell function characterize bone marrow of HIV-infected subjects with low CD4R T cell counts despite viral suppression during HAART. Clin Infect Dis 2008; 46:1902-1910.